Environmental Pollution 252 (2019) 1483e1490 Contents lists available at ScienceDirect Environmental Pollution journal homepage: www.elsevier.com/locate/envpol Biological consequences of environmental pollution in running water ecosystems: A case study in zooplankton* * Wei Xiong a, Ping Ni a, b, Yiyong Chen a, b, Yangchun Gao a, b, Shiguo Li a, b, Aibin Zhan a, b, a Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, 18 Shuangqing Road, Haidian District, Beijing 100085, China b University of Chinese Academy of Sciences, Chinese Academy of Sciences, 19A Yuquan Road, Shijingshan District, Beijing 100049, China article info abstract Article history: Biodiversity in running water ecosystems such as streams and rivers is threatened by chemical pollution Received 19 February 2019 derived from anthropogenic activities. Zooplankton are ecologically indicative in aquatic ecosystems, Received in revised form owing to their position of linking the top-down and bottom-up regulators in aquatic food webs, and thus 10 June 2019 of great potential to assess ecological effects of human-induced pollution. Here we investigated the Accepted 12 June 2019 influence of water pollution on zooplankton communities characterized by metabarcoding in Songhua Available online 24 June 2019 River Basin in northeast China. Our results clearly showed that varied levels of anthropogenic distur- bance significantly influenced water quality, leading to distinct environmental pollution gradients Keywords: < Water pollution (p 0.001), particularly derived from total nitrogen, nitrate nitrogen and pH. Redundancy analysis fi fl Biodiversity showed that such environmental gradients signi cantly in uenced the geographical distribution of Metabarcoding zooplankton biodiversity (R ¼ 0.283, p ¼ 0.001). In addition, along with the trend of increasing envi- Songhua River Basin ronmental pollution, habitat-related indicator taxa were shifted in constituents, altering from large-sized Zooplankton species (e.g. arthropods) in lightly disturbed areas to small-sized organisms (e.g. rotifers and ciliates) in highly disturbed areas. All these findings clearly showed that anthropogenic activity-derived water pollution significantly influenced biological communities. Thus, biotic consequences of human-induced environmental pollution in running water ecosystems should be deeply investigated. More impor- tantly, the findings of biotic consequences should be well integrated into existing monitoring programs to further assess impacts of anthropogenic disturbance, as well as to advance the management of running water ecosystems for conservation and ecological restoration. © 2019 Elsevier Ltd. All rights reserved. 1. Introduction and domestic sewage and run-offs from farmlands in their vast basins (Pander and Geist, 2013; Xiong et al., 2016b). In order to Anthropogenic disturbance, such as release of chemical pollut- assess environmental deterioration of habitat condition caused by ants, has influenced freshwater ecosystems globally by causing chemical pollution, the degree and spatial/temporal variation of habitat degradation and biodiversity loss (Meybeck and Helmer, physicochemical parameters have been measured in many routine 1989; Vor€ osmarty€ et al., 2010), and further greatly compromised monitoring programs, and the contribution of various chemicals to the functioning and service of aquatic ecosystems (Dudgeon et al., water quality has been well evaluated in numerous rivers and 2006; Woodward et al., 2012). It is well-known that running water streams (e.g. Jiang et al., 2018; Wijesiri et al., 2018; Zhang et al., ecosystems such as streams and rivers harbor an extremely high 2019). Compared with the well-investigated contribution of level of biodiversity (Vor€ osmarty€ et al., 2010). Unfortunately, rivers chemical pollution to habitat deterioration, biotic responses to and streams are among the most vulnerable habitats as they water pollution remain largely unexplored in anthropogenic extensively receive anthropogenic disturbance, such as industrial activity-influenced habitats, particularly for microscopic organisms at the community level (but see Wang et al., 2010; García-Chicote et al., 2017; Zhao et al., 2017). However, biotic responses to * This paper has been recommended for acceptance by Maria Cristina Fossi. human-induced water pollution are at the core of environmental * Corresponding author. Research Center for Eco-Environmental Sciences, Chi- degradation assessment in aquatic ecosystems, as biological com- nese Academy of Sciences, 18 Shuangqing Road, Haidian District, Beijing 100085, munities are a direct endpoint of increasing environmental stresses China. E-mail addresses: [email protected], [email protected] (A. Zhan). and biological integrity is a crucial component of ecosystem health https://doi.org/10.1016/j.envpol.2019.06.055 0269-7491/© 2019 Elsevier Ltd. All rights reserved. 1484 W. Xiong et al. / Environmental Pollution 252 (2019) 1483e1490 (Jeppesen et al., 2011). In addition, understanding the influence of zooplankton communities. Metabarcoding produces huge biodi- anthropogenic disturbance on aquatic communities is essential to versity information of complex communities with high sensitivity develop effective restoration plans and conduct sound manage- and resolution (Ji et al., 2013; Zhan et al., 2013). Additionally, ment for running water ecosystems (Hering et al., 2006; Pander and metabarcoding enables detection of cryptic species, species at Geist, 2013). larval stage and species that are either too rare, small or fragile to be Among many microscopic communities in running water eco- investigated by traditional morphological identification (Zhan et al., systems, zooplankton play fundamental roles in energy transfer 2014; Zhan and MacIsaac, 2015; Xiong et al., 2016a). Thus, meta- and nutrient cycle due to their pivotal positions in aquatic food barcoding represents a powerful tool to address the influence of webs (Du et al., 2015; García-Chicote et al., 2017). In addition, increasing human disturbance on zooplankton communities. In this zooplankton have been considered as one of the earliest and most study, we investigated biological consequences of water pollution sensitive taxonomic groups during processes of environmental in SRB in northeast China, using zooplankton communities char- changes, such as dynamics of trophic states in aquatic ecosystems acterized by metabarcoding as a case study. We firstly discerned (Schindler, 1987; Lin et al., 2017). Several studies have demon- major environmental pollutants that contributed to the variation of strated that environmental filtering caused by local environmental environmental conditions along gradients of anthropogenic pollution was a dominant mechanism on constraining zooplankton disturbance. Secondly, we investigated the influence of environ- communities in highly polluted running water ecosystems at a mental pollution on the variation of zooplankton communities. single river scale (Xiong et al., 2017; Yang et al., 2018), as distinct Finally, we identified indicator taxa in habitats influenced by environmental variation was easy to form by frequent human different levels of anthropogenic disturbance and further analyzed disturbance at a fine geographical scale (Heino et al., 2015). Thus, variation of these taxa along disturbance gradients. the dynamics of environment-driven community assembly makes zooplankton good indicators for assessing community-level re- 2. Materials and methods sponses to environmental degradation caused by anthropogenic disturbance (Attayde and Bozelli, 1998; Ismail and Mohd Adnan, 2.1. Field sampling 2016). In addition, environmental factors responsible for commu- nity variation varied when different rivers were investigated, as In order to investigate impacts of water pollution derived from each river was influenced by different types of human disturbance varied levels of anthropogenic disturbance, we sampled Upper (e.g. Xiong et al., 2016b, 2017; Zhao et al., 2017; Peng et al., 2018). Songhua River and Songhua River in forest, rural and agriculture, Thus, it is crucial to identify river-specific environmental stressors and urban areas (Fig. 1) in July 2017. We sorted these sampling sites that have influenced spatial and temporal succession dynamics of into the less disturbed area (LDA), intermediately disturbed area communities, particularly for critical rivers that support various (IDA) and highly disturbed area (HDA) based on land use types. In types of industries but have been highly disturbed by intensive total, we chose and sampled 23 sites, including 5, 11, and 7 in LDA, anthropogenic activities. IDA and HDA, respectively (Fig. 1). Songhua River Basin (SRB), extending from 41.7 to 51.8N and For each sampling site, three parallel surface water samples from 119.9 to 132.5E in the northeast of China and covering an (10 L) were collected, pooled together and filtered through a 25-mm area of approximately 556,800 km2, has three main reaches: Upper mesh net to collect quantitative zooplankton samples in 20 min. All Songhua River, Songhua River and Nen River (Ma et al., 2013). collected zooplankton samples were preserved instantly in the field Upper Songhua River is 958 km long and covers a total area of 73, in 100 mL anhydrous alcohol. Meanwhile, for water quality mea- 400 km2 (Fig.1). Songhua River, which is located in the downstream surement, 500 mL water samples were collected at each sampling of Upper Songhua River, starts from the convergence of Upper site.